ER-aminopeptidase 1 determines the processing and presentation of an immunotherapy-relevant melanoma epitope.
Aminopeptidases
/ immunology
Antigen Presentation
/ immunology
Antigens, Neoplasm
Cell Line, Tumor
Endoplasmic Reticulum
/ immunology
Epitopes, T-Lymphocyte
/ immunology
HeLa Cells
Humans
Immunologic Factors
/ immunology
Immunotherapy
/ methods
Melanoma
/ immunology
Minor Histocompatibility Antigens
/ immunology
Peptides
/ immunology
Proteasome Endopeptidase Complex
/ immunology
T-Lymphocytes
/ immunology
CD8+ T cells
ER-aminopeptidase
gp100
melanoma
proteasome
Journal
European journal of immunology
ISSN: 1521-4141
Titre abrégé: Eur J Immunol
Pays: Germany
ID NLM: 1273201
Informations de publication
Date de publication:
02 2020
02 2020
Historique:
received:
22
01
2019
revised:
19
08
2019
accepted:
13
11
2019
pubmed:
16
11
2019
medline:
14
7
2020
entrez:
16
11
2019
Statut:
ppublish
Résumé
Dissecting the different steps of the processing and presentation of tumor-associated antigens is a key aspect of immunotherapies enabling to tackle the immune response evasion attempts of cancer cells. The immunodominant glycoprotein gp100
Identifiants
pubmed: 31729751
doi: 10.1002/eji.201948116
doi:
Substances chimiques
Antigens, Neoplasm
0
Epitopes, T-Lymphocyte
0
Immunologic Factors
0
Minor Histocompatibility Antigens
0
Peptides
0
Aminopeptidases
EC 3.4.11.-
ERAP1 protein, human
EC 3.4.11.-
Proteasome Endopeptidase Complex
EC 3.4.25.1
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
270-283Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : SFB-TR36
Pays : International
Organisme : Deutsche Krebshilfe
ID : Nr. 106861
Pays : International
Organisme : Berliner Krebsgesellschaft e.V.
ID : Z:SEFF200907
Pays : International
Organisme : AICE FIRE Onlus Emilia Romagna
Pays : International
Organisme : CRUK - KHP Centre at King's College London
Pays : International
Organisme : King's College London - Monash University
Pays : International
Informations de copyright
© 2019 The Authors. European Journal of Immunology published by WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim.
Références
Rosenberg, S. A. and Restifo, N. P., Adoptive cell transfer as personalized immunotherapy for human cancer. Science 2015. 348: 62-68.
Coulie, P. G., Van den Eynde, B. J., van der Bruggen, P. and Boon, T., Tumour antigens recognized by T lymphocytes: at the core of cancer immunotherapy. Nat. Rev. Cancer 2014. 14: 135-146.
Ritz, D., Gloger, A., Weide, B., Garbe, C., Neri, D. and Fugmann, T., High-sensitivity HLA class I peptidome analysis enables a precise definition of peptide motifs and the identification of peptides from cell lines and patients' sera. Proteomics 2016. 16: 1570-1580.
Liepe, J., Marino, F., Sidney, J., Jeko, A., Bunting, D. E., Sette, A., Kloetzel, P. M. et al., A large fraction of HLA class I ligands are proteasome-generated spliced peptides. Science 2016. 354: 354-358.
Mishto, M. and Liepe, J., Post-translational peptide splicing and T cell responses. Trends Immunol. 2017. 38: 904-915.
Strehl, B., Seifert, U., Kruger, E., Heink, S., Kuckelkorn, U. and Kloetzel, P. M., Interferon-gamma, the functional plasticity of the ubiquitin-proteasome system, and MHC class I antigen processing. Immunol. Rev. 2005. 207: 19-30.
Guillaume, B., Chapiro, J., Stroobant, V., Colau, D., Van Holle, B., Parvizi, G., Bousquet-Dubouch, M. P. et al., Two abundant proteasome subtypes that uniquely process some antigens presented by HLA class I molecules. Proc. Natl. Acad. Sci. U. S. A. 2010. 107: 18599-18604.
Zanker, D., Waithman, J., Yewdell, J. W. and Chen, W., Mixed proteasomes function to increase viral peptide diversity and broaden antiviral CD8+ T cell responses. J. Immunol. 2013. 191: 52-59.
Klare, N., Seeger, M., Janek, K., Jungblut, P. R. and Dahlmann, B., Intermediate-type 20 S proteasomes in HeLa cells: “asymmetric” subunit composition, diversity, and adaptation. J. Mol. Biol. 2007. 373: 1-10.
Mishto, M., Liepe, J., Textoris-Taube, K., Keller, C., Henklein, P., Weberruss, M., Dahlmann, B. et al., Proteasome isoforms exhibit only quantitative differences in cleavage and epitope generation. Eur. J. Immunol. 2014. 44: 3508-3521.
Kincaid, E. Z., Che, J. W., York, I., Escobar, H., Reyes-Vargas, E., Delgado, J. C., Welsh, R. M. et al., Mice completely lacking immunoproteasomes show major changes in antigen presentation. Nat. Immunol. 2011. 13: 129-135.
Chapiro, J., Claverol, S., Piette, F., Ma, W., Stroobant, V., Guillaume, B., Gairin, J. E. et al., Destructive cleavage of antigenic peptides either by the immunoproteasome or by the standard proteasome results in differential antigen presentation. J. Immunol. 2006. 176: 1053-1061.
Guillaume, B., Stroobant, V., Bousquet-Dubouch, M. P., Colau, D., Chapiro, J., Parmentier, N., Dalet, A. et al., Analysis of the processing of seven human tumor antigens by intermediate proteasomes. J. Immunol. 2012. 189: 3538-3547.
Kuckelkorn, U., Stubler, S., Textoris-Taube, K., Killian, C., Niewienda, A., Henklein, P., Janek, K. et al, Proteolytic dynamics of human 20S thymoproteasome. J. Biol. Chem. 2019. 294: 7740-7754.
Liepe, J., Holzhutter, H. G., Bellavista, E., Kloetzel, P. M., Stumpf, M. P. and Mishto, M., Quantitative time-resolved analysis reveals intricate, differential regulation of standard- and immuno-proteasomes. Elife 2015.4.
Seifert, U., Maranon, C., Shmueli, A., Desoutter, J. F., Wesoloski, L., Janek, K., Henklein, P. et al., An essential role for tripeptidyl peptidase in the generation of an MHC class I epitope. Nat. Immunol. 2003. 4: 375-379.
Saveanu, L., Carroll, O., Lindo, V., Del Val, M., Lopez, D., Lepelletier, Y., Greer, F. et al., Concerted peptide trimming by human ERAP1 and ERAP2 aminopeptidase complexes in the endoplasmic reticulum. Nat. Immunol. 2005. 6: 689-697.
Tanioka, T., Hattori, A., Masuda, S., Nomura, Y., Nakayama, H., Mizutani, S. and Tsujimoto, M., Human leukocyte-derived arginine aminopeptidase. The third member of the oxytocinase subfamily of aminopeptidases. J. Biol. Chem. 2003. 278: 32275-32283.
Cifaldi, L., Romania, P., Lorenzi, S., Locatelli, F. and Fruci, D., Role of endoplasmic reticulum aminopeptidases in health and disease: from infection to cancer. Int. J. Mol. Sci. 2012. 13: 8338-8352.
Fruci, D., Ferracuti, S., Limongi, M. Z., Cunsolo, V., Giorda, E., Fraioli, R., Sibilio, L. et al., Expression of endoplasmic reticulum aminopeptidases in EBV-B cell lines from healthy donors and in leukemia/lymphoma, carcinoma, and melanoma cell lines. J. Immunol. 2006. 176: 4869-4879.
Stoehr, C. G., Buettner-Herold, M., Kamphausen, E., Bertz, S., Hartmann, A. and Seliger, B., Comparative expression profiling for human endoplasmic reticulum-resident aminopeptidases 1 and 2 in normal kidney versus distinct renal cell carcinoma subtypes. Int. J. Clin. Exp. Pathol. 2013. 6: 998-1008.
York, I. A., Brehm, M. A., Zendzian, S., Towne, C. F. and Rock, K. L., Endoplasmic reticulum aminopeptidase 1 (ERAP1) trims MHC class I-presented peptides in vivo and plays an important role in immunodominance. Proc. Natl. Acad. Sci. U. S. A. 2006. 103: 9202-9207.
James, E., Bailey, I., Sugiyarto, G. and Elliott, T., Induction of protective antitumor immunity through attenuation of ERAAP function. J. Immunol. 2013. 190: 5839-5846.
Keller, M., Ebstein, F., Burger, E., Textoris-Taube, K., Gorny, X., Urban, S., Zhao, F. et al. The proteasome immunosubunits, PA28 and ER-aminopeptidase 1 protect melanoma cells from efficient MART-126-35 -specific T-cell recognition. Eur. J. Immunol. 2015. 45: 3257-3268.
Mpakali, A., Maben, Z., Stern, L. J. and Stratikos, E., Molecular pathways for antigenic peptide generation by ER aminopeptidase 1. Mol. Immunol. 2019. 113: 50-57.
Stratikos, E., Stamogiannos, A., Zervoudi, E. and Fruci, D., A role for naturally occurring alleles of endoplasmic reticulum aminopeptidases in tumor immunity and cancer pre-disposition. Front. Oncol. 2014. 4: 363.
Evnouchidou, I., Weimershaus, M., Saveanu, L. and van Endert, P., ERAP1-ERAP2 dimerization increases peptide-trimming efficiency. J. Immunol. 2014. 193: 901-908.
Chen, H., Li, L., Weimershaus, M., Evnouchidou, I., van Endert, P. and Bouvier, M., ERAP1-ERAP2 dimers trim MHC I-bound precursor peptides; implications for understanding peptide editing. Sci. Rep. 2016. 6: 28902.
Blees, A., Januliene, D., Hofmann, T., Koller, N., Schmidt, C., Trowitzsch, S., Moeller, A. et al., Structure of the human MHC-I peptide-loading complex. Nature 2017. 551: 525-528.
Blum, J. S., Wearsch, P. A. and Cresswell, P., Pathways of antigen processing. Annu. Rev. Immunol. 2013. 31: 443-473.
Kawakami, Y., Eliyahu, S., Jennings, C., Sakaguchi, K., Kang, X., Southwood, S., Robbins, P. F. et al., Recognition of multiple epitopes in the human melanoma antigen gp100 by tumor-infiltrating T lymphocytes associated with in vivo tumor regression. J. Immunol. 1995. 154: 3961-3968.
Smith, F. O., Downey, S. G., Klapper, J. A., Yang, J. C., Sherry, R. M., Royal, R. E., Kammula, U. S. et al., Treatment of metastatic melanoma using interleukin-2 alone or in conjunction with vaccines. Clin. Cancer Res. 2008. 14: 5610-5618.
Rosenberg, S. A., Yang, J. C., Schwartzentruber, D. J., Hwu, P., Marincola, F. M., Topalian, S. L., Restifo, N. P. et al., Immunologic and therapeutic evaluation of a synthetic peptide vaccine for the treatment of patients with metastatic melanoma. Nat. Med. 1998. 4: 321-327.
Schwartzentruber, D. J., Lawson, D. H., Richards, J. M., Conry, R. M., Miller, D. M., Treisman, J., Gailani, F. et al., gp100 peptide vaccine and interleukin-2 in patients with advanced melanoma. N. Engl. J. Med. 2011. 364: 2119-2127.
Textoris-Taube, K., Keller, C., Liepe, J., Henklein, P., Sidney, J., Sette, A., Kloetzel, P. M. et al., The T210M substitution in the HLA-a*02:01 gp100 epitope strongly affects overall proteasomal cleavage site usage and antigen processing. J. Biol. Chem. 2015. 290: 30417-30428.
Bakker, A. B., Schreurs, M. W., Tafazzul, G., de Boer, A. J., Kawakami, Y., Adema, G. J. and Figdor, C. G., Identification of a novel peptide derived from the melanocyte-specific gp100 antigen as the dominant epitope recognized by an HLA-A2.1-restricted anti-melanoma CTL line. Int. J. Cancer 1995. 62: 97-102.
Mishto, M., Goede, A., Taube, K. T., Keller, C., Janek, K., Henklein, P., Niewienda, A. et al., Driving forces of proteasome-catalyzed peptide splicing in yeast and humans. Mol. Cell. Proteomics 2012. 11: 1008-1023.
Dalet, A., Robbins, P. F., Stroobant, V., Vigneron, N., Li, Y. F., El-Gamil, M., Hanada, K. I. et al., An antigenic peptide produced by reverse splicing and double asparagine deamidation. Proc. Natl. Acad. Sci. U. S. A. 2011. 108: E323-E331.
Dalet, A., Stroobant, V., Vigneron, N. and Van den Eynde, B. J., Differences in the production of spliced antigenic peptides by the standard proteasome and the immunoproteasome. Eur. J. Immunol. 2011. 41: 39-46.
Ebstein, F., Textoris-Taube, K., Keller, C., Golnik, R., Vigneron, N., Van den Eynde, B. J., Schuler-Thurner, B. et al., Proteasomes generate spliced epitopes by two different mechanisms and as efficiently as non-spliced epitopes. Sci. Rep. 2016. 6: 24032.
Michaux, A., Larrieu, P., Stroobant, V., Fonteneau, J. F., Jotereau, F., Van den Eynde, B. J., Moreau-Aubry, A. et al., A spliced antigenic peptide comprising a single spliced amino acid is produced in the proteasome by reverse splicing of a longer peptide fragment followed by trimming. J. Immunol. 2014. 192: 1962-1971.
Platteel, A. C., Mishto, M., Textoris-Taube, K., Keller, C., Liepe, J., Busch, D. H., Kloetzel, P. M. et al., CD8 T cells of Listeria monocytogenes-infected mice recognize both linear and spliced proteasome products. Eur. J. Immunol. 2016. 46: 1109-1118.
Platteel, A. C. M., Liepe, J., Textoris-Taube, K., Keller, C., Henklein, P., Schalkwijk, H. H., Cardoso, R. et al., Multi-level strategy for identifying proteasome-catalyzed spliced epitopes targeted by CD8+ T cells during bacterial infection. Cell Rep. 2017. 20: 1242-1253.
Vigneron, N., Stroobant, V., Chapiro, J., Ooms, A., Degiovanni, G., Morel, S., van der Bruggen, P. et al., An antigenic peptide produced by peptide splicing in the proteasome. Science 2004. 304: 587-590.
Warren, E. H., Vigneron, N. J., Gavin, M. A., Coulie, P. G., Stroobant, V., Dalet, A., Tykodi, S. S. et al., An antigen produced by splicing of noncontiguous peptides in the reverse order. Science 2006. 313: 1444-1447.
Tenzer, S., Wee, E., Burgevin, A., Stewart-Jones, G., Friis, L., Lamberth, K., Chang, C. H. et al., Antigen processing influences HIV-specific cytotoxic T lymphocyte immunodominance. Nat. Immunol. 2009. 10: 636-646.
Deol, P., Zaiss, D. M., Monaco, J. J. and Sijts, A. J., Rates of processing determine the immunogenicity of immunoproteasome-generated epitopes. J. Immunol. 2007. 178: 7557-7562.
Mehta, A. M., Jordanova, E. S., van Wezel, T., Uh, H. W., Corver, W. E., Kwappenberg, K. M., Verduijn, W. et al., Genetic variation of antigen processing machinery components and association with cervical carcinoma. Genes Chromosomes Cancer 2007. 46: 577-586.
Yao, Y., Wisniewski, A., Ma, Q., Kowal, A., Porebska, I., Pawelczyk, K., Yu, J. et al., Single nucleotide polymorphisms of the ERAP1 gene and risk of NSCLC: a comparison of genetically distant populations, Chinese and Caucasian. Arch. Immunol. Ther. Exp. (Warsz) 2016. 64: 117-122.
Reeves, E., Elliott, T., Edwards, C. J. and James, E., Both rare and common ERAP1 allotypes have distinct functionality defined by polymorphic context and are important in AS association. Proc. Natl. Acad. Sci. U. S. A. 2017. 114: E1575-E1576.
Hodi, F. S., O'Day, S. J., McDermott, D. F., Weber, R. W., Sosman, J. A., Haanen, J. B., Gonzalez, R. et al., Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 2010. 363: 711-723.
McDermott, D., Haanen, J., Chen, T. T., Lorigan, P., O'Day, S. and Investigators, M. D. X., Efficacy and safety of ipilimumab in metastatic melanoma patients surviving more than 2 years following treatment in a phase III trial (MDX010-20). Ann. Oncol. 2013. 24: 2694-2698.
Mehta, A. M., Osse, M., Kolkman-Uljee, S., Fleuren, G. J. and Jordanova, E. S., Molecular backgrounds of ERAP1 downregulation in cervical carcinoma. Anal. Cell. Pathol. (Amst) 2015. 2015: 367837.
Vigneron, N., Ferrari, V., Van den Eynde, B. J., Cresswell, P. and Leonhardt, R. M., Cytosolic processing governs TAP-independent presentation of a critical melanoma antigen. J. Immunol. 2018. 201: 1875-1888.
Ugurel, S., Thirumaran, R. K., Bloethner, S., Gast, A., Sucker, A., Mueller-Berghaus, J., Rittgen, W. et al., B-RAF and N-RAS mutations are preserved during short time in vitro propagation and differentially impact prognosis. PLoS One 2007. 2: e236.
Kuckelkorn, U., Frentzel, S., Kraft, R., Kostka, S., Groettrup, M. and Kloetzel, P. M., Incorporation of major histocompatibility complex-encoded subunits LMP2 and LMP7 changes the quality of the 20S proteasome polypeptide processing products independent of interferon-gamma. Eur. J. Immunol. 1995. 25: 2605-2611.
Urban, S., Textoris-Taube, K., Reimann, B., Janek, K., Dannenberg, T., Ebstein, F., Seifert, C. et al., The efficiency of human cytomegalovirus pp65(495-503) CD8+ T cell epitope generation is determined by the balanced activities of cytosolic and endoplasmic reticulum-resident peptidases. J. Immunol. 2012. 189: 529-538.
Ebstein, F., Lange, N., Urban, S., Seifert, U., Kruger, E. and Kloetzel, P. M., Maturation of human dendritic cells is accompanied by functional remodelling of the ubiquitin-proteasome system. Int. J. Biochem. Cell Biol. 2009. 41: 1205-1215.
Oh, I. S., Textoris-Taube, K., Sung, P. S., Kang, W., Gorny, X., Kahne, T., Hong, S. H. et al., Immunoproteasome induction is suppressed in hepatitis C virus-infected cells in a protein kinase R-dependent manner. Exp. Mol. Med. 2016. 48: e270.
Gohlke, S., Kloss, A., Tsokos, M., Textoris-Taube, K., Keller, C., Kloetzel, P. M. and Dahlmann, B., Adult human liver contains intermediate-type proteasomes with different enzymatic properties. Ann. Hepatol. 2014. 13: 429-438.
Liepe, J., Mishto, M., Textoris-Taube, K., Janek, K., Keller, C., Henklein, P., Kloetzel, P. M. et al., The 20S proteasome splicing activity discovered by SpliceMet. PLoS Comput. Biol. 2010. 6: e1000830.
Cox, J., Hein, M. Y., Luber, C. A., Paron, I., Nagaraj, N. and Mann, M., Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol. Cell. Proteomics 2014. 13: 2513-2526.
Kieback, E., Charo, J., Sommermeyer, D., Blankenstein, T. and Uckert, W., A safeguard eliminates T cell receptor gene-modified autoreactive T cells after adoptive transfer. Proc. Natl. Acad. Sci. U. S. A. 2008. 105: 623-628.
Yao, Y., Liu, N., Zhou, Z. and Shi, L., Influence of ERAP1 and ERAP2 gene polymorphisms on disease susceptibility in different populations. Hum. Immunol. 2019. 80: 325-334.